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The effect of grazing by large herbivores on the diversity of plant communities has been investigated in different terrestrial ecosystems (Milchunas & Lauenroth 1993; Proulx & Mazumder 1998). Grazing increased, reduced or lacked consistent effect on plant diversity (Huston 1994; Proulx & Mazumder 1998). These contrasting patterns of response have frequently been attributed to differences in grazing intensity, with greatest diversity expected at intermediate levels of grazing (Grime 1973; Connell 1978). More recent research, however, has shown that characteristics of the ecosystem that is subjected to grazing, such as primary productivity, evolutionary history and resulting vegetation physiognomy and plant life-forms, can interact with grazing in determining plant community structure and diversity (Whittaker 1977; Huston 1979, 1994; Milchunas et al. 1988; Milchunas & Lauenroth 1993; Noy-Meir 1995; Proulx & Mazumder 1998). Among these characteristics, primary productivity is particularly important as it determines both standing biomass and extent of grazing, while at the same time it modulates plant interactions and is linked to community structure (Waide et al. 1999; Grace & Jutila 1999). Furthermore, across plant communities, primary productivity is a comparable indicator of spatial and temporal variation in resource availability. Productivity–diversity relationships have been studied in varied ecosystems, with unimodal, positive and negative relationships frequently emerging (Grace & Jutila 1999; Waide et al. 1999; Gross et al. 2000). Usually, diversity is low in environments with very low availability of resources (i.e. where few species can survive) and increases with increasing resource availability. In contrast, diversity tends to decline in high productivity environments, due to competitive exclusion by favoured species that became abundant under these conditions (Grime 1973, 1979; Keddy 1990; Huston 1994). The significance of competition for generating productivity–diversity relationships in low-productivity systems is, however, not yet clear (Goldberg & Novoplansky 1997).
The impact of grazing on diversity differs along gradients of primary productivity (Milchunas et al. 1988; Louda et al. 1990; Okansen 1990), but there is no general consensus about the processes involved in this interaction. Competitive relationships among plants depend on resource availability. In environments with high resource availability and productivity, plants will be more likely to compete for canopy resources (light), while in less productive environments plant growth and diversity will be limited by soil resources (water, minerals) (Tilman 1982, 1988; Kadmon 1995). Shifts in the relative availability of canopy vs. soil resources might modulate interspecific competition and therefore the outcome of grazing effects on community structure. In his ‘dynamic equilibrium model of species diversity’Huston (1979) predicted that grazing can change diversity in opposite ways in resource-poor vs. resource-rich ecosystems, and this was supported by the meta-analysis performed over a wide variety of environments by Proulx & Mazumder (1998) (their grazing reversal hypothesis). Furthermore, based on a world-wide data-set analysis, Milchunas & Lauenroth (1993) proposed that alteration in grassland structure and diversity due to grazing was primarily a function of productivity and evolutionary grazing history of each particular grassland ecosystem. These factors determine species composition and the prevailing life-forms and morphological traits that characterize the plant community. This, in turn, dictates the responses of individual species to grazing.
The interaction between grazing and primary productivity on species diversity has been mostly studied at the ecosystem level, in perennial grasslands (Milchunas & Lauenroth 1993). In contrast to perennial grasslands, annual grasslands lack temporal continuity in their competitive interactions. Furthermore, in perennial grasslands the window of relaxed competitive interaction after disturbance is mainly a consequence of plant regrowth capabilities, while annual grasslands depend more on seed-bank dynamics and seedling establishment (Briske & Noy-Meir 1998). We asked if the relationships found between diversity, productivity and grazing in perennial grasslands are operative also in annual grasslands, particularly in low productivity, semiarid regions. The herbaceous communities in Mediterranean semiarid rangelands offer an excellent opportunity to study this question, as they have been used for grazing since historical times and are dominated by annual species, many of them tolerant to grazing (Noy-Meir & Seligman 1979; Le Houerou 1993; Shmida & Ellner 1983; Perevolotsky & Seligman 1998). Annuals are widespread in Mediterranean rangelands and well adapted to semiarid ecosystems (Shmida & Burgess 1988), in which primary productivity is usually limited by seasonality in soil resources, mainly water and nitrogen (Seligman & van Keulen 1989). Furthermore, the typical heterogeneity of annual rainfall and habitat topography in semiarid regions often results in a highly patchy distribution of these limiting resources (Noy-Meir 1973). This heterogeneity, together with the dynamic nature of annual plant populations that regenerate every year from the available seed-bank, can cause wide spatial and temporal variation in primary productivity.
In this study, we propose that the Milchunas et al. (1988) general model developed for geographically separated ecosystems (i.e. large scale) differing in primary productivity, also applies to local fine scales. We hypothesize that in Mediterranean semiarid regions, in which annual plants are the main primary biomass producers, changes in community diversity in response to grazing will depend on small-scale variation of productivity in time and space. More specifically, we asked: (i) Does the productivity-richness relationship vary between topographic sites and between years that differ in productivity? (ii) Does the extent and direction of change in richness caused by grazing depend on small-scale temporal and spatial variation in productivity? (iii) Which components of species richness contribute to such changes in diversity? These questions were studied in a long-term experiment in a semiarid rangeland in Israel, by comparing the responses of annual plant communities to protection from grazing in neighbouring topographic sites that differ in primary productivity.
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Primary productivity of the annual plant community in this Mediterranean semiarid rangeland varied strongly through time and space, with water availability as a main driving factor, as found in other semiarid regions (Noy-Meir 1973; Le Houerou 1993). The temporal and spatial variation in productivity was mainly due to interannual differences in precipitation (40–247 mm year−1), and to heterogeneity in water run-off/run-on and physical characteristics among the topographic sites. During the study period, the above-ground productivity at peak season in the subplots protected from grazing in the hilltop, and south- and north-facing slopes was 10–200 g m−2, a range typical of semiarid ecosystems. In contrast, productivity in the wadi shoulders reached up to 700 g m−2, within the range for subhumid grassland ecosystems (Milchunas et al. 1988), although productivity in drier years (< 200 g m−2) was more characteristic of semiarid ecosystems. Within this productivity gradient, grazing increased richness in the high productivity site (wadi shoulders), but did not affect or reduced it in the low productivity sites (Fig. 2). This reversal in richness as a function of productivity was predicted and therefore provides further support to the dynamic equilibrium model (Huston 1979), Milchunas et al.'s (1988) generalized model and the grazing reversal hypothesis (Proulx & Mazumder 1998). Although it can be argued that the different effects of grazing at high productivity could be attributed to their intrinsically higher grazing intensity, this intensity was not correlated with the extent of change in richness across our productivity gradient. Higher diversity in grazed vs. ungrazed grasslands has also been reported for Mediterranean regions with higher rainfall and greater productivity (Naveh & Whittaker 1979; Noy-Meir et al. 1989; Montalvo et al. 1993; Hadar et al. 2000; Sternberg et al. 2000), as well as in coastal meadows (Grace & Jutila 1999) and other grassland systems (Waser & Price 1981; Pucheta et al. 1998; Dupre & Diekman 2001).
The opposite effects of grazing on species richness observed along the productivity gradient can be interpreted as the outcome of the interaction between grazing, resource availability and plant competition for different limiting resources, as shown in the conceptual model in Fig. 6. A basic assumption is that, at the low productivity (< 200 g m−2), plant growth and diversity is limited by soil resources (mainly water and minerals), while at higher levels of productivity, leading to larger above-ground biomass, competition is mainly for canopy resources (Tilman 1982, 1988; Milchunas et al. 1988). Thus, in the low productivity range, in which the gradual increase in richness can be related to increasing availability of soil resources, richness was either unaffected or slightly reduced by grazing, most likely due to plant removal and trampling (Noy-Meir 1990). At higher levels of productivity (such as in the wadi), species richness continues to rise under grazing, probably in response to larger soil resources and to a parallel reduction of competition for light, due to removal by grazing of the palatable larger species. Without grazing, on the other hand, richness did not continue to increase in the higher productivity range and was generally lower than in the grazed subplots. This lack of increase could result from greater competition for canopy resources (i.e. light) and displacement of smaller, less competitive species (Grime 1979; Huston 1994). All together, these trends can be interpreted as a reversal in richness due to grazing along a productivity gradient, in which plant competition shifts from below-ground to above-ground resources. Despite the widely held assumption that grazing lowers competition intensity, few studies actually examined the impact of grazing on competitive interactions among plants (Goldberg & Barton 1992; Taylor et al. 1997), and none of them have considered annual plant communities along gradients of productivity.
Figure 6. Conceptual model of the relationship between small-scale variation in productivity and richness of annual species in a grazed or ungrazed semiarid Mediterranean rangeland.
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Milchunas et al. (1988) suggested that the shift from competition for soil resources to competition for canopy resources that occurs with increasing productivity might explain the differences in the response to grazing found between semiarid and subhumid grasslands. Our data suggest that this shift also explains the interaction between grazing and small-scale variation in productivity that determines species richness in heavily grazed annual plant communities in semiarid Mediterranean rangelands possessing high spatial and temporal heterogeneity in resource availability. Our small-scale conceptual model corresponds to the large-scale model proposed by Milchunas et al. (1988) for semiarid to subhumid ecosystems of perennial grasslands with a long history of grazing. It is important to note that, in contrast to the Milchunas et al. generalized model, which compared distinct communities occurring along geographical gradients in productivity, we compared neighbouring sites whose annual plant communities were relatively similar before the establishment of the exclosures. Sorenson's index of similarity among the high (wadi) and low productivity sites (hilltop, and north- and south-facing slopes), as well as among the low productivity sites themselves, was 0.5–0.6 (Osem et al., unpublished results). This further supports our conclusion that the changes in richness due to protection from grazing were due mainly to differences in productivity of the topographic sites and not to initial floristic differences in their annual plant communities.
Contrary to expectations, richness did not decrease at high productivity levels in the absence of grazing and the richness–productivity relationship was not therefore unimodal across sites and years. However, unimodal relationships have been found in other semiarid plant communities with comparable ranges of productivity, including some in the Mediterranean region (Kutiel & Danin 1986; Puerto et al. 1990). In a comparable study in a transition zone between grassland and shrubland in Arizona in which annuals are dominant, the hump-shaped relationship was detected only when very diverse microhabitats (open sites, ant and rat mounds, and shrub fertility islands) were pooled together in the analysis (Guo & Berry 1998). In the Chihuahua Desert, sites protected from grazing and with higher productivity due to additional ‘run-on’ were found to be overwhelmingly dominated by a single species and exhibited lower diversity, compared with less productive sites (Ludwig 1986). These facts suggest that a unimodal curve emerges when wide ranges of the environmental productivity gradient are integrated (Rosenzweig 1995; Pausas 2001). The large variation in species richness observed in the ungrazed subplots in the wadi (the most productive site) rather than the expected decrease suggests that other processes are masking the richness–productivity relationship. Possible explanations for this large variation in richness are the relatively short time that has elapsed since exclosures were established in 1993 and variation in the rate of recovery of the annual vegetation of different plots after cessation of grazing. Analysis of soil samples from the wadi site showed that seed density of the larger and palatable grasses and legumes in the grazed subplots is very low, due to intensive grazing and limited dispersal of their seeds (Osem et al., unpublished data). This may have resulted in a patchy distribution of the larger species during the initial stages of recovery after fencing, with their distribution becoming more homogeneous with time. Thus, if rate of recovery differs among the high productivity plots, it is conceivable that in plots in which the seed density of the larger and palatable species is still relatively low, the competitive displacement of the smaller species will be less intense, and richness in these plots will be higher. Additionally, a persistent seed bank of the less competitive species may lead to their slower decline in the vegetation after fencing, thus maintaining a higher diversity. It can be argued that, in annual grasslands, variation in species richness after cessation of grazing is modulated by initial seed density constraints and by a balance between the seed-bank dynamics of the different species. These trends in the vegetation and in the seed-bank most probably affect the relationship between productivity and richness during recovery from grazing, with the hump-shaped relationship emerging after longer periods of protection from grazing. Local deficiency of seeds has been proposed as an important factor in generating small-scale vegetation patterns in calcareous grasslands (Zobel et al. 2000; Turnbull et al. 2000).
The changes in richness that were observed in different plots along the productivity gradient could be attributed to variation in plant density, as increasing plant density should increase the probability of finding additional species. Indeed, the density vs. productivity relationships were similar to those observed for richness vs. productivity. However, the richness vs. density relationships were weaker compared with the richness vs. productivity relationships. Furthermore, the large variation in richness observed in the high productivity subplots protected from grazing was not related to density, thus indicating the involvement of other processes.
Analysis of the components of species richness revealed a consistent increase in rare species across the range of productivity, whereas numbers of abundant and common species remained relatively constant. The effects of productivity and grazing on the small-scale temporal and spatial diversity of the annual plant community were therefore due to variation in the number of less abundant species. It can be argued that variation in the presence of species is limited by their availability at a regional scale (the regional species pool; Zobel 1997; Grace 2001). Indeed, the study area is surrounded by grazed land with similar vegetation, from which species with low tolerance to grazing disappeared long ago. Moreover, dispersal capability of most species in the region (except a few composites with wind dispersal) is quite limited (Ellner & Shmida 1981; Osem et al., unpublished data). Therefore, short-term changes in the annual vegetation after grazing exclusion are less likely to be due to colonization by propagules originating from the regional species pool, but rather to result from shifts in the relative proportion of species initially present in the local, small-scale species pool. This pool is maintained in the seed-bank of the grazed area and in natural refuges protecting from grazing, such as rock outcrops and shrubs. In the Spanish dehesa annual pastures, rare species (representing 47% of the total richness) are assumed to persist in the community as a result of their persistent seed-banks, which allow establishment and production of fresh seed input in rainy (i.e. highly productive) years (Peco et al. 1998). It is conceivable that the establishment and reproductive success of species from the local pool is controlled by abiotic (i.e. resource availability) and biotic (i.e. grazing, competition) factors that operate at the small spatial-scale, and whose relative importance changes along the productivity gradient. Within this context, it can be argued that less abundant species are more susceptible to availability of resources and grazing (Zobel et al. 2000). Indeed, the number of the abundant species along the productivity gradient was relatively small and constant. Thus, in this semiarid Mediterranean rangeland with winter rains, diversity of the annual plant community is mainly determined by the less abundant species, due to the interaction between grazing and small-scale temporal and spatial variation in primary productivity.